Journal of Threatened Taxa | www.threatenedtaxa.org | 26 October 2013 | 5(14): 4840–4853 Article Biology of the Mountain Crayfish Euastacus sulcatus Riek, 1951 (Crustacea: Parastacidae), in New South Wales, Australia
Jason Coughran ISSN Online 0974–7907 Print 0974–7893 jagabar Environmental, PO Box 634, Duncraig, Western Australia, 6023, Australia [email protected] OPEN ACCESS
Abstract: The biology and distribution of the threatened Mountain Crayfish Euastacus sulcatus, was examined through widespread sampling and a long-term mark and recapture program in New South Wales. Crayfish surveys were undertaken at 245 regional sites between 2001 and 2005, and the species was recorded at 27 sites in the Clarence, Richmond and Tweed River drainages of New South Wales, including the only three historic sites of record in the state, Brindle Creek, Mount Warning and Richmond Range. The species was restricted to highland, forested sites (220–890 m above sea level), primarily in national park and state forest reserves. Adult crayfish disappear from the observable population during the cooler months, re-emerging in October when the reproductive season commences. Females mature at approximately 50mm OCL, and all mature females engage in breeding during a mass spawning season in spring, carrying 45–600 eggs. Eggs take six to seven weeks to develop, and the hatched juveniles remain within the clutch for a further 2.5 weeks. This reproductive cycle is relatively short, and represents a more protracted and later breeding season than has been inferred for the species in Queensland. A combination of infrequent moulting and small moult increments indicated an exceptionally slow growth rate; large animals could feasibly be 40–50 years old. Implications for the conservation and management of E. sulcatus are discussed.
Keywords: Conservation, Euastacus, IUCN, growth, moulting, reproduction, spiny crayfish, subtropical rainforest, threatened species.
Abbreviations:AbGR - absolute growth rate; AbW - abdominal width; NP - National Park; NSW - New South Wales; OCL - orbital carapace length (see Morgan 1997); PCMI - percent moult increment; PropL - propodal length; SF - State Forest
DOI: http://dx.doi.org/10.11609/JoTT.o3647.4840-53 | ZooBank: urn:lsid:zoobank.org:pub:A250C1DA-124E-4742-B1D8-697DABEE542D
Editor: Tadashi Kawai, Wakkanai Fisheries Research Institute, Hokkaido, Japan. Date of publication: 26 October 2013 (online & print)
Manuscript details: Ms # o3647 | Received 01 June 2013 | Final received 02 October 2013 | Finally accepted 05 October 2013
Citation: Coughran, J. (2013). Biology of the Mountain CrayfishEuastacus sulcatus Riek, 1951 (Crustacea: Parastacidae), in New South Wales, Australia. Journal of Threatened Taxa 5(14): 4840–4853; http://dx.doi.org/10.11609/JoTT.o3647.4840-53
Copyright: © Coughran 2013. Creative Commons Attribution 3.0 Unported License. JoTT allows unrestricted use of this article in any medium, reproduction and distribution by providing adequate credit to the authors and the source of publication.
Funding: Funding was provided by Southern Cross University, the Australian Geographic Society, and jagabar Environmental.
Competing Interest:Author declare no competing interests.
Author Details: Jason Coughran completed a PhD in Biology at Southern Cross University in 2006, and his research interests are the biology, ecology, taxonomy and conservation of aquatic fauna, with a focus on inland systems. He is currently engaged in these fields through a private research and consulting entity, jagabar Environmental.
Acknowledgements: This work was undertaken during my postgraduate research at Southern Cross University, and I thank my supervisor Don Gartside and the technical staff who assisted me: Craig Taylor, Max Egan, Maxine Dawes, Peter Bligh-Jones and Roz Hagan. Research funds were provided by Southern Cross Uni- versity and the Australian Geographic Society. Amy Coughran, Andy Moore, Ben Black, David Newell, Paul Collins, Shawn Leckie and Stephen Waddington assisted with field work for this species, and the National Parks and Wildlife Service, NSW Fisheries and State Forests of NSW departments provided scientific collection permission. I thank Jagabar Environmental for providing me with time to prepare the manuscript, and two anonymous reviewers for their constructive comments.
4840 Biology of Euastacus sulcatus Coughran
INTRODUCTION Queensland (Furse & Wild 2002a,b, 2004; Furse et al. 2004, 2006), its NSW distribution is unclear. Further, Edgar Riek (1951) formally described the Mountain many biological aspects remain undocumented Crayfish, Euastacus sulcatus, from over one hundred including: (i) the incidence of wounds and disease; (ii) specimens collected from Tamborine Mountain reproductive biology details; and (iii) wild moulting and and Lamington National Park (NP) in southeastern growth increments. In this paper, I present the findings Queensland, Australia. In the same paper, Riek also of a detailed biological research program encompassing described E. cunninghami from Cunningham’s Gap. both broad field surveys in NSW, and a two-year mark These taxa were distinguished largely on the basis that and recapture program examining the biology of E. E. cunninghami was more setose and had reduced sulcatus. abdominal spination. However, it subsequently became apparent that these two species were conspecific, and the latter was synonymised with E. sulcatus by Morgan METHODS (1988). The collections by Morgan (1988) also provided Field surveys were undertaken at 245 sites across a more complete understanding of the distribution northeastern NSW between 2001 and 2005, with the for E. sulcatus, extending in an arc from Tambourine aim of thoroughly describing the taxonomy, distribution, Mountain to the Lamington Plateau, westwards along habitat and ecology of all regional crayfish species the McPherson Range bordering New South Wales (Coughran 2006a). Sampling was undertaken via NSW (NSW), and north again to the Mistake Mountains. He Scientific Collection permits, and the NSW National recorded the species from only two NSW sites, at Brindle Parks and Wildlife Service’s (2001) Frog Hygiene Protocol Creek and Mount Warning (Morgan 1988). The species was followed throughout the study. Crayfish were was subsequently recorded further west in NSW, on collected by hand or hand net, with baited string lines the Richmond Range (Leckie 1999; Coughran 2000), or traps (with meat baits), or by lifting rocks and other prompting a comprehensive research program on its debris and probing burrows by hand. Both diurnal and distribution, taxonomy, biology and ecology (Coughran nocturnal surveys were undertaken, and observations 2006a). were made of crayfish activity, conspecific interactions Euastacus sulcatus is a large, spiny crayfish species, and the presence of wounds and disease. Habitat reaching up to 340mm in overall length, and 425g in characteristics and basic water quality parameters (pH, weight (Furse & Wild 2004). The species differs from conductivity, dissolved oxygen and temperature) were most other large, spiny species of Euastacus, including recorded throughout the study. E. suttoni and E. valentulus in the immediate region, in that it lacks thoracic spines. It is also regionally unique Population Study: Brindle Creek (Images 1 & 2) because it exhibits marked base colour variation: for In addition to data collected from surveys across the example, specimens from the Lamington Plateau and species’ NSW range, a long-term monitoring site was Springbrook in Queensland are blue, while specimens established at Brindle Creek, in the World Heritage listed from Brindle Creek and the Richmond Range in NSW Border Ranges NP (Fig. 1). The site comprised typical are typically red (Morgan 1988; Coughran 2000, Brindle Creek habitat, the predominant locality of three 2006a,b). In addition to its striking colouration, large historic sites of record for the species in NSW, and size and impressive spination, E. sulcatus has become sufficiently far away (and upstream) from the popular an iconic species for park visitors, due to its tendency to recreational part of the park to avoid visitor impacts. periodically wander around on forest floors (Riek 1951; The site encompassed a stream length of approximately Morgan 1991; Furse & Wild 2002b; Furse et al. 2004). 500m. Despite the above, several knowledge gaps remain The creek at this site was relatively large, reaching for this species, which has recently been formally widths of 5–10 m, and with pools often 1–2 m deep. recognised as Endangered on the IUCN Red List of There was a permanent flow in the creek, and all Threatened Species (Furse & Coughran 2010). Filling sections retained some surface water throughout the these knowledge gaps is of fundamental importance to sampling period. The substratum was generally fine, but ensuring the conservation of this species. For example, also incorporated a coarser component of gravelly sand although the ecology and population characteristics in places. There was moderate to dense cobble and of E. sulcatus have been relatively well studied in boulder cover in most of the larger pools, in which rocks
Journal of Threatened Taxa | www.threatenedtaxa.org | 26 October 2013 | 5(14): 4840–4853 4841 Biology of Euastacus sulcatus Coughran
Figure 1. The NSW distribution of the Mountain Crayfish,Euastacus sulcatus, was greatly extended during the study (new sites indicated with stars), and the species was also recorded at all previously known sites (circles). Distinct NSW populations are numbered, as follows: 1 - Mount Warning; 2 - Nightcap; 3 - Border Ranges (including Brindle Creek); 4 - Toonumbar; 5 - Richmond Range; 6 - Yabbra (north); 7 - Yabbra (south); 8 - Koreelah. Known sites of record from Queensland are represented by circles.
Image 1. Mountain Crayfish Euastacus sulcatus in natural habitat Image 2. Natural habitat of Euastacus sulcatus (03.ii.2002, © Jason (23.iv.2003, © Jason Coughran, Brindle Creek). Coughran, Brindle Creek).
4842 Journal of Threatened Taxa | www.threatenedtaxa.org | 26 October 2013 | 5(14): 4840–4853 Biology of Euastacus sulcatus Coughran were sparsely distributed, often in small aggregations. moult events. Two methods of growth rate estimation The banks were generally gentle to moderate in slope, were applied to the mark-recapture data: although in some stretches the banks were steep, and - Percent Moult Increment (PCMI) was combined occasionally vertical. The site received a moderate with an estimate of moult frequency to estimate growth amount of sunlight, but submerged aquatic plants were (Hamr & Richardson 1994; Hamr 1997; Borsboom 1998); absent. Exposed rocks in the stream bed, however, were and often covered with semi-aquatic plants such as Rainforest - Absolute Growth Rate (AbGR), taken as the change Spinach Elatostema reticulatum. The surrounding forest in OCL since last capture divided by the number of was subtropical rainforest. months since last capture (Lake & Sokol 1986).
Marking Maturity The Brindle Creek crayfish population was sampled The gonopores of female crayfish were examined monthly from August 2001 to July 2003. Animals were for secondary sexual characteristics, including: marked with a unique identifier using the tailfan clipping development of setae around the female gonopores; the code of Coughran (2011a). Some animals with damaged level of inflation of the gonopores in comparison to the tailfans were not clippable and were excluded from surrounding coxal surface; and whether gonopores were marking. A small number of aggressively protective still calcified or membranous. These data were used to berried females were not marked, to avoid disturbing assign maturity stages, similar to those established for the clutch. Generally, however, berried females were Euastacus bispinosus by Honan & Mitchell (1995c), as marked. All crayfish marked at the long-term monitoring follows: site were returned to the water at the point of capture. - Immature: Gonopores small, level with surrounding Crayfish were measured with vernier calipers to the coxal surface, and calcified; nearest 0.1mm for OCL and abdominal width (Morgan - Adolescent: Rim of gonopore incised, a few setae 1997). Both chelae were also measured for propodal may be present on the coxal surface surrounding the length, width and depth. Chelae were considered normal gonopore, often the gonopore is slightly darker than the (i.e., non-regenerate) when they differed by <1mm surrounding coxal surface, sometimes decalcified but propodal length from their counterpart; otherwise they not raised or membranous; and were noted as slightly regenerate (1–3 mm smaller) - Mature: Gonopore decalcified, fleshy looking and or distinctly regenerate (>3mm smaller than their raised like a blister above the surrounding coxal surface, counterpart). often fringed by dense setae.
Density Relative abdominal width (i.e., AbW/OCL) and chela Crayfish density (per linear m of stream) at the Brindle size (i.e., PropL/OCL) have also been used as secondary Creek site was estimated from the mark-recapture data, indicators of sexual maturity (Honan & Mitchell 1995c; using three multiple census equations: Hamr 1997). It has been noted in other species that - the original and adjusted Schnabel methods males develop proportionally larger chelae, and females (Schnabel 1938; Chapman 1952); and develop proportionally larger abdomens, as they - the Schumaker method (Ricker 1975). mature. Comparisons of these measurements for male and female E. sulcatus were analysed and tested for Animals that were captured more than one time significance with the normal probability density function during a monthly session were considered once only in and Student’s t test. the population estimates. Some animals were excluded from the analyses, including specimens <15mm OCL, Egg Size, Fecundity and Spawning and specimens that were badly injured during collection. For all females carrying eggs or juveniles (i.e., “berried”), fecundity was estimated in the field, and Growth and Moulting up to 20 eggs were retained from selected crayfish for Crayfish were designated to have an ‘exoskeleton subsequent laboratory measurement (total sample: 163 condition’, as described by Coughran (2011a), and a eggs taken from 24 females). The retained eggs were subsequent change in exoskeleton condition was used examined using a dissecting microscope, photographed to verify moult events for recaptured individuals. Where and measured. Mean egg sizes (egg width, measured possible, pereiopod regeneration was also used to verify across the shortest axis; and egg length, measured
Journal of Threatened Taxa | www.threatenedtaxa.org | 26 October 2013 | 5(14): 4840–4853 4843 Biology of Euastacus sulcatus Coughran across the longest axis) were calculated, and ratios of crayfish from eastern Mount Warning had turquoise egg width/OCL and egg length/OCL were determined. shields over a red base colour, and those from Yabbra To complement field observations of reproductive had tan shields over a very dark brown (almost black) activity, three ovigerous females were retained from base colour (Images 3 & 4). The extent of development the wild and maintained in laboratory aquaria. The of the shields varied considerably, and in some cases laboratory was permanently air-conditioned to 022 C, dominated the colour of the animal. Photographs of and water temperatures in the aquaria generally these various colour forms of E. sulcatus in NSW have remained within 1–2 0C of this throughout the study. been provided elsewhere (Coughran 2006b). Female crayfish were provided with a leaf litter and sand substrate with rock, decaying wood and pipe General Ecology shelters, and supplemental food in the form of algae The species occurred in rainforest habitats, or wet pellets and flaked food. Two or three eggs, or juveniles, sclerophyll forest with gallery rainforest along the stream were removed from the reproductive females twice margins, in national parks or relatively undisturbed areas weekly, and examined under a dissecting microscope of state forests with similar habitat. One exception was and photographed. The entire clutch of eggs, or a private site where the species was recorded in a minor juveniles, was also photographed periodically during the gully lacking surface water, within a small (i.e., ~20m x developmental period. 20m) remnant patch of gallery rainforest. Otherwise, Independent juveniles were grown in matured 80 litre aquaria, with a substrate of sand, gravel and leaf litter from their wild habitat. Long maturation had enabled an algal growth and invertebrate fauna to develop in these aquaria, and the juvenile crayfish were provided with minimal supplemental food.
RESULTS
Distribution Euastacus sulcatus was recorded at 27 sites, including the three NSW historical sites. The species distribution was substantially extended south along the Tweed Range, southeast along the Nightcap Range and on Mt Warning, and westward along the McPherson Range to Image 3. Euastacus sulcatus blue and cream form Brummies Creek Koreelah NP (Fig. 1). The species is now known to occur (06.ix.2002, © Jason Coughran) in the Tweed, Richmond and Clarence River drainages of northeastern NSW, and is relatively widespread in this state. Although the species was morphologically similar across its range, and generally consistent with the current taxonomic description (Morgan 1988), colouration varied markedly between the different populations across its distribution. Most western populations (e.g., Border Ranges, Richmond Range, Koreelah) displayed a red base colour, as is also common in western Queensland (Coughran, unpub. data). In the Nightcap Range, crayfish had a blue base colour, previously thought restricted to south-eastern Queensland (Furse & Wild 2002a). Large animals from all populations in the species’ range had the prominent pale patches, or “shields”, on the abdomen, carapace and chelae that is characteristic of the species. Image 4. Euastacus sulcatus red and turquoise form Korrumbyn These shields were usually a cream colour, however Creek eastern Mt Warning (13.iv.2002 © Jason Coughran)
4844 Journal of Threatened Taxa | www.threatenedtaxa.org | 26 October 2013 | 5(14): 4840–4853 Biology of Euastacus sulcatus Coughran the species was recorded from publicly managed areas, 81.1mm) recorded by Morgan (1988). The smallest including Border Ranges, Koreelah, Mount Warning, trapped animal was 20.8mm OCL, and the smallest Nightcap, Richmond Range, Toonumbar and Yabbra caught by hand was 7.5mm OCL. NPs, and Whian Whian, Wollumbin and Yabbra SFs. The One-hundred-and-ninety-nine animals were marked species was found at altitudes above 220m, extending at the Brindle Creek site. Thirty-one of these (15.6%) upwards to 890m. were recaptured at least once, with seven recaptured The species inhabited a wide variety of aquatic and twice or more (up to a maximum of nine recaptures). semi-aquatic habitats, from moist gullies with no surface The mean monthly recapture rate was 13%. The water to large, flowing streams. The conductivity was estimated crayfish density at the site was approximately relatively low (<350µS/cm), the pH ranged from 6.08– 1.5 crayfish per linear metre (Table 1). 8.04, and the water temperature ranged from 7–24 0C. The minimum dissolved oxygen concentration recorded Wounds and Disease was 6.08mg/L. The substrate varied from fine silt to Wounds were recorded on 98 crayfish (32.6%) gravel. Where cover was found in the form of rocks from the Brindle Creek site, and 37 crayfish (37.0%) and woody and leafy debris, the species commonly from other sites. In addition to missing or damaged excavated burrows into the stream bed. Burrows were pereiopods, wounds were most commonly recorded also common in stream banks and in the adjacent forest in the cephalothorax, rostrum and chelae. Seventeen floor. In large streams, wide burrows and pits were animals had burn spot disease on the carapace or excavated in banks and beneath boulders and logs, chelae. One adult female (69.3mm OCL) had a small from which numerous animals of varying sizes were carapace wound, and when recaptured one month later, often lured out. It therefore appeared that the species its carapace had mostly deteriorated on one side, leaving had both communal and solitary habits. Burrows in the the gills completely exposed. The crayfish appeared stream bed not associated with cover were less common. behaviorally unaffected by this substantial wound, and it was observed actively hunting in the stream before Activity being recaptured. Except for small juveniles, crayfish were absent Ten animals (<2.5%) sacrificed a chela during from the stream during the cooler months, from April handling, and these were excluded from the following to October. When the animals returned in the warmer analyses. Only 52.7% of the animals from Brindle Creek months, the mature females were berried. bore two normal chelae. Approximately 5.7% of animals Euastacus sulcatus were mostly diurnal, and during were either missing a chela or bore only soft chela buds, the months when animals were more active they were 18.2% had a distinctly regenerate chela and 23.3% had a commonly encountered. Crayfish were commonly slightly regenerate chela. observed transiting the forest, particularly during wet weather. During high stream flow periods some animals Moulting were engaged in harvesting vegetation (e.g., moss or Animals in the process of moulting were commonly riparian plants), or carrying washed out vegetation captured from within burrows under rocks. Several or small pieces of tree-falls back to their burrows. animals were also observed moulting in shallow waters Throughout the active months, E. sulcatus were readily of the open stream, usually on a rock top. Because most trapped or lured out of burrows; if direct bait access was crayfish were absent from the water body during the impossible animals often partially consumed any trap- winter months, the records of moulting were considered associated materials (e.g., hessian, stockings, plastic, unreliable for defining a growing season. netting, ropes or floats).
Population Study: Brindle Creek Table 1. Estimates of population density for Euastacus sulcatus from In total, 301 animals from the Brindle Creek site the long-term biological monitoring site at Brindle Creek (site length 500m). (including recaptured animals), and a further 100 crayfish per crayfish from other sites in the broad distribution Estimation Method N 95% CL surveys, were measured and examined. A maximum linear metre size of 90.8mm OCL was recorded for E. sulcatus at the Schnabel 784.97 561.87–1135.7 1.57 Brindle Creek site, and 99.5mm OCL at other sites. This Schnabel (modified) 762.54 548.03–1098.31 1.53 was considerably larger than the maximum OCL (i.e., Schumaker 736.66 550.08–1114.78 1.47
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Table 2. Growth and moulting records for recaptured Euastacus sulcatus, from Brindle Ck, and determination of the PCMI (%) and AbGR
(mm/month) for OCL. C»R, earliest and latest months of capture and recapture for each growth interval; tm, time in months between capture records; Moults*, estimated number of moults between records; Initial, OCL prior to moulting (mm); Final, OCL after moulting (mm); MI, moult increment (mm). Two entries marked * are for the same individual, which moulted twice during the study, and was recaptured and measured each time.
C » R tm Moults* Initial Final MI PCMI AbGR Females
Feb-Oct 8 1 53.1 57.4 4.3 8.1 0.5
Nov-Oct 11 1 70.9 73.4 2.5 3.5 0.2
Nov-Oct 11 1 67.6 69.2 1.6 2.4 0.1
Nov-Feb 15 1 57.0 60.8 3.8 6.7 0.3
Mean (Female) 5.2 0.3
Males
Nov-Feb 3 1 52.8 56.8 4.0 7.6 1.3
Nov-May* 6 1 54.4 58.5 4.1 7.5 0.7
Nov-May 6 1 60.0 64.6 4.6 7.7 0.8
Aug-Feb 6 1 75.6 77.9 2.3 3.0 0.4
Aug-Mar 7 1 46.6 51.0 4.4 9.4 0.6
Nov-Nov* 12 1 49.1 54.4 5.3 10.8 0.4
May-Jun 13 1 76.1 78.2 2.1 2.8 0.2
Jan-Feb 13 1 61.6 65.0 3.4 5.5 0.3
Mar-May 14 1 72.0 73.6 1.6 2.2 0.1
Jan-Oct 21 1 81.5 83.6 2.1 2.6 0.1
Mean (Male) 5.9 0.5
Mean (Overall) 5.7 0.4
Only 13 of the 31 recaptured Euastacus sulcatus the AbGR ranged between 0.1 and 0.4 mm/month moulted between captures, although one of these (Table 2). Eighteen Euastacus sulcatus were recaptured animals moulted twice during the study (and was that displayed no growth between captures. The time captured and measured at each moult). Thus, there intervals between captures for these animals ranged up were 14 growth records for E. sulcatus (Table 2). Most to eight months (generally between 3 to 4 months, but of these recaptures were over long periods, providing including four records over five months), and extended some useful insights into the growth of this species. The across all seasons. moult increment in E. sulcatus appears to be correlated with size. Animals <50mm OCL had PCMIs (for OCL) of Reproductive Biology around 10%, animals from 50–60 mm OCL had PCMIs Sexual dimorphism was evident in a proportionally of 6.7–8.1%, and animals over 60mm OCL had PCMIs larger propodal length (i.e., larger chelae; student’s t of 2.2–5.5%. This trend of decreasing growth with test, p<0.001) in males, and a broader abdomen (normal increasing size can be seen in one male animal for which probability density function, p<0.0001) in females (Table two years of moulting records are available. In the first 3). Three specimens were observed with aberrant year of records, it increased from 49.1–54.4 mm OCL sexual characteristics. These included one specimen (PCMI 10.8%), and in the second year it increased a with two male gonopores and one female gonopore, further 4.1–58.5 mm OCL, representing a lower PCMI and two specimens with only a single female gonopore (7.5%). (i.e., gonopore present on one side only). The 13 Euastacus sulcatus animals that had been Females generally reached sexual maturity at or recaptured over periods of six months or more had above 50mm OCL (Fig. 2), although two females were AbGRs (for OCL) of less than 1mm/month. For the six recorded with mature gonopore states at considerably animals recaptured over periods of 12 months or more, smaller sizes (23.7mm, 28.8mm). An aberrant female
4846 Journal of Threatened Taxa | www.threatenedtaxa.org | 26 October 2013 | 5(14): 4840–4853 Biology of Euastacus sulcatus Coughran
20
15
n 10
5
0
OCL (mm) Figure 2. Number of immature (white), adolescent (grey) and mature OCLfemale (mm) (black) Euastacus sulcatus from the long-term monitoring site at Brindle Creek as determined by gonopore state.
Table 3. Sexual dimorphism for E. sulcatus animals (>50 mm OCL) from the long-term monitoring site at Brindle Creek: i) relative eggs or juveniles when captured. These females abdomen width (AbW/OCL); and ii) relative propodal length (PropL/ OCL). F = female; M = male; NPDF = normal probability density ranged from 51.5–90.4 mm OCL, and the clutches were function. estimated to contain between 45–600 eggs. The egg AbW/OCL PropL/OCL length was approximately 5–8 % of the OCL of the female Sex F M F M carrying them; the mean egg length was 4.09mm, and the mean egg width was 3.19mm. mean ratio 0.53 0.47 0.81 0.87 The berried females were in variable condition n 76 66 39 24 with regard to wounds; two females had at least one S.D. 0.091 0.019 0.020 0.046 chela missing (one had both chelae missing), 25 had S.E. 0.011 0.01 a regenerate chela; and two had other missing or Student's test NPDF regenerate pereiopods. Other wounds recorded on t-test berried females included tailfan damage (2), burn spot p <0.0001 <0.001 (2), and broken or regenerate dactylar or propodal fingers (4). Forty-six of the 48 females (95.8%) had very clean exoskeleton states. Thirteen of the 48 females of 41.5mm OCL also had mature gonopores. Ten carried brown and/or white temnocephalan flatworms. females >50mm OCL had immature (6) or adolescent (4) The timing of reproductive activity for the48 gonopore characteristics. All females >65mm OCL were berried E. sulcatus females (Fig. 3) clarified this as a sexually mature. The mean AbW/OCL ratio for mature, late spring-summer brooder, with release of juveniles female E. sulcatus was 0.55 (n = 66), and 0.50 for both in early summer. Most females over the minimum size immature (n = 42) and adolescent (n = 19) animals. at egg bearing (51.5mm) that were captured during this Forty-eight Euastacus sulcatus females were carrying reproductive season were carrying eggs or young.
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50
45
40
35
30
n 25
20
15
10
5
0 Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
Month Figure 3. Reproductive activity forEuastacus sulcatus females above the minimum size at egg bearing (OCL 51.5 mm), by month of capture: without eggs or juveniles (white); carrying eggs (grey); and (iii) carrying juveniles (black).
Egg and Juvenile Development regional species, and has been described and illustrated The initial stages of egg development could not be elsewhere (Coughran 2006a). recorded, due to the absence of adults from the water Eggs began hatching 35 days after capture, indicating during the cooler months. Compared to observations a total gestation time of approximately 42–49 days for egg development in three other regional species (assuming the eggs were between 7–14 days old at (Coughran 2006a, 2011a,b), it was estimated that the time of capture). The hatchling crayfish remained eggs were one to two weeks old when the females re- connected to the egg case by a telson thread, and the appeared in spring. egg cases remained cemented to the pleopodal setae of Throughout the broad distribution surveys, the mother; these two connections provided a means undeveloped eggs (lacking any internal development) of anchoring the hatchlings to the mother, in a clutch were only observed on a few specimens collected at carried beneath her abdomen. At least two moults were Grady’s Creek, in the Border Ranges NP, in 2003. At evident while juveniles remained within the clutch, this site, adults were found carrying eggs at varying and independence from the mother was observed developmental stages (even on the same individual), approximately 2.5 weeks after hatching. and it was estimated that the eggs had been laid within Juveniles were characterized by distinctive cream the past week or two. On the same day, Brindle Creek bands across the first and last abdominal segments. was sampled and adults had also returned to the water, Many independent juvenile Euastacus sulcatus from red but as in other years, females were found to be carrying colour form populations (Brindle Creek) developed into eggs that were more advanced in development than the blue colour form while in captivity, perhaps due to a those on the females at Grady’s Creek; moreover, egg plant-based diet (supplemental algae pellets). All of the development at Brindle Creek was more even between captive juveniles also developed the prominent cream different females (and estimated at more than two shields that in the wild were generally only observed on weeks old). adults. The eggs of E. sulcatus were ovoid in shape and, prior to the yolk darkening, were opaque and pale orange-tan in colour. The yolk changed to a translucent red-brown, pink-red or orange-red colour as the yolk developed. A detailed sequence of egg development was observed that was consistent with observations for other
4848 Journal of Threatened Taxa | www.threatenedtaxa.org | 26 October 2013 | 5(14): 4840–4853 Biology of Euastacus sulcatus Coughran
DISCUSSION for many non-Australian species (Somers & Stechey 1986; Matthews & Reynolds 1995; Riggert et al. 1999) Distribution and General Ecology and for Australian genera such as Cherax (Geddes 1990), The Clarence River valley in NSW forms the other spiny crayfish such asE. armatus and E. bispinosus boundary between Euastacus sulcatus and E. suttoni. have been observed to be winter active species (Geddes The systematic relationship between these two taxa 1990; Honan & Mitchell 1995a). However, Barker (1992) is uncertain and they may fill similar niches in their noted both daily and seasonal differences in catchability respective environments. They are both large, spiny between three species of Euastacus, and had to modify species, and their general morphological attributes his survey methods accordingly. Sampling in the are certainly more similar to each other than to other traditional Victorian crayfishing season (winter), he regional crayfishes. Euastacus sulcatus is widespread in readily caught E. armatus but had to postpone sampling montane habitats east of the Clarence River valley, while for E. kershawi until later in the year. E. suttoni is similarly widespread in montane habitats to Monroe (1977) and Borsboom (1998) observed a the west. Neither species was recorded from the lower, tendency for Euastacus robertsi and E. urospinosus to more central habitats of the river valley. sit at burrow entrances at night, which is suggestive Several poorly spinose species of Euastacus were of a nocturnal nature. However, E. sulcatus was sympatric with E. sulcatus, including E. angustus, E. predominantly diurnal, with greater numbers observed binzayedi, E. dalagarbe, E. girurmulayn, E. guruhgi, E. and caught during the day. Diurnal activity has also been jagabar, E. jagara and E. maidae. All of these species recorded for Queensland populations, and is discussed belong within a different ecomorphological group of further elsewhere (Coughran 2006a; Furse et al. 2006). the genus (Coughran’s Group 1) to E. sulcatus (Group The tendency of Euastacus sulcatus to leave the 2) (Coughran 2008). The larger Euastacus sulcatus water and walk about on land has also been reported dominated sympatric associations, usually excluding the for this and other Euastacus species (Flecker & Flecker smaller species from the main channel or the deeper 1936; Clark 1937; Riek 1959; Morey & Hollis 1997; sections of streams. However, small E. sulcatus animals Morey 1998; Furse et al. 2004). One reason for this were also recorded in the peripheral habitats, tributaries would appear to be food acquisition; in several cases, E. and gullies occupied by these smaller species. Therefore, sulcatus individuals were foraging on (or in) the riparian specimens of E. sulcatus and these smaller Euastacus mosses and macrophytes near the water’s edge. In spp. were often collected together, and occasionally other cases, crayfish were found some distance from the from under the same rock. Conversely, Euastacus water (up to around 100m), on leaf litter on the forest sulcatus appears to be mutually exclusive with crayfish floor. On one occasion, a colleague observed a large E. from within its ecomorphological group (Group 2). The sulcatus on the forest floor feeding on a deceased sugar species occurs in close proximity to E. gumar and clearly glider (David Newell, Southern Cross University, pers. overlaps with E. valentulus in some areas, but it did not comm. 2004). co-occur with these species. Many crayfish were recaptured from the immediate area in which they had been previously released, as Activity much as 21 months earlier, suggesting that despite If temperature is a limiting factor for E. sulcatus, their propensity for substantial overland and in-stream restricting it to higher altitudes (as has been suggested movement, they show high burrow fidelity, with a for highland species of Euastacus generally; e.g., Riek well-established and permanent burrow to which 1969; Horwitz 1990; Merrick 1993; Morgan 1997; they continue to return. Long term studies on other Coughran & Furse 2010), then the habit of the species Euastacus species have reported similar findings: Honan to disappear from the observable population over the & Mitchell (1995a) found most E. bispinosus moved <75 cooler months of the year is most unusual. This pattern m during their study, and Morey (1998) recaptured E. would be expected for a species occurring near its lower, kershawi animals in the same vicinity up to four years not upper, thermal threshold. Furse et al. (2006) also after release. recorded this for Queensland populations of E. sulcatus, however the re-emergence of adults in their study Moulting, Growth and Longevity (December to January) was notably later than during the The apparently decreasing moult increment with present study (October). increasing size is commonly reported for crustaceans Although reduced winter activity has been observed (Hartnoll 1983), but is not consistent with E. sulcatus
Journal of Threatened Taxa | www.threatenedtaxa.org | 26 October 2013 | 5(14): 4840–4853 4849 Biology of Euastacus sulcatus Coughran laboratory growth studies by Furse & Wild (2004), approximation of age for these species difficult. Juveniles who found moult increment increased with increasing that survived in aquaria grew at varying rates, although crayfish size. These contrasting findings might be due noticeably slower (~15–20 mm OCL in 18 months) than to differences between the source populations, or two congeners that were studied concurrently, E. gumar more likely the effects of the laboratory conditions on and E. valentulus. It is likely that juveniles in the wild captive animals in their study. In other species, moult also exhibit different growth rates. increments and/or growth generally for laboratory Based on the growth rates observed in captivity, it animals have been found to be higher (e.g., Jones 1981), would be a reasonable assumption that wild animals at similar (e.g., Turvey & Merrick 1997b) or lower (e.g., around 25mm OCL could be anywhere from 2–4 years Tulonen et al. 1995) than for wild animals. old. Studies on other Euastacus have also indicated The mark-recapture work suggests that Euastacus that at least two to three years would be required to sulcatus animals >45mm OCL only moult annually, and attain 25mm OCL (Turvey & Merrick 1997c; Borsboom potentially less often in substantially larger animals. A 1998; Furse & Wild 2004). If this is so, then based on number of individuals caught several times during the the observed moult increments of typically 2–4 mm in study, including an 81.5mm OCL male recaptured nine this study, it is likely that E. sulcatus animals at 50mm times across 21 months, supported these findings. All OCL (the size at female maturity) could be at least 8–10 six animals that were recaptured after periods of 12 years old. Animals at 70mm OCL could easily be over 20 months or more (ranging up to 21 months) appeared to years old. have moulted only once. There were further indications The lower moult increments observed in animals of infrequent moulting in the apparently non-growing above this size (approximately 1–2 mm) suggest that specimens that were recaptured, with intervening growth from 70–90 mm OCL could take a further 10–20 periods of up to eight months without moult, and a years. This slow development was also clearly expressed low incidence of recently moulted animals captured in the AbGRs for four animals >70mm OCL, over periods throughout the study. Furse & Wild (2004) also recorded of more than 12 months. At a growth rate of 0.1–0.2 long intermoult periods for E. sulcatus (i.e., up to 821 mm per month, an increase in OCL from 70–99 mm days). could be expected to take 12 to 24 years. At 99.1mm The potentially longer than annual moulting interval OCL, the largest animal recorded could have conceivably for large E. sulcatus is similar to findings for the large been in the vicinity of 40 to 50 years old. spiny crayfish E. bispinosus and E. kershawi, for which Like those recorded for E. gumar (Coughran 2011a), no moulting, or moults with an insignificant increment, these AbGRs are extremely low, and suggest that these have been recorded (Honan & Mitchell 1995b; Morey animals would require around three years to increase 1998). Some of the moult increments recorded in the <15 mm in OCL (and for larger animals, <10mm). These present study were so small that they could essentially be AbGRs are also much lower than those recorded for considered as negligible (and for such small increments Cherax destructor by Lake & Sokol (1986); although the measuring error also limits accuracy). It may be the there are fewer data in the present study, the time spans case that for large animals, moulting is undertaken to between captures are much longer than those available produce a clean exoskeleton, and/or to rehabilitate limbs for Lake & Sokol’s (1986) study, and reflect growth over or wounds, rather than necessarily increasing in size. annual time scales. If non-moulting animals had been The high incidence of wounds in this species suggests included in the analysis, the AbGRs for this species that aggressive interactions are common; repairing this would have been far lower than those presented. physical damage and regenerating limbs would require While these long term growth records clearly indicate considerable redirection of energy resources that would greater longevity than Furse et al. (2004) predicted for otherwise be available for growth. The high proportion Queensland animals (i.e., 17 years), further research is of clean exoskeleton states also suggests that, in general, needed to obtain more precise growth and longevity females moult prior to spawning. estimates. Similar to other crustaceans (Hartnoll 1983), A wide range of age estimates have been reported the combination of infrequent moult intervals with for other large Euastacus (e.g., 22–39 years for 110–120 exceptionally small moult increments substantially mm OCL E. spinifer; Turvey & Merrick 1997c), and the limited the effectiveness of indirect age and growth moult increment variation in the present study similarly estimation methods for this species. Therefore, for presents difficulty for E. sulcatus age estimation. slow-growing and long-lived species like E. sulcatus, The paucity of juvenile growth data also makes the direct ageing methods would be ideal and could
4850 Journal of Threatened Taxa | www.threatenedtaxa.org | 26 October 2013 | 5(14): 4840–4853 Biology of Euastacus sulcatus Coughran potentially resolve the uncertainties mentioned here; their conspicuous presence, ease of capture (they can recent advances in ageing studies have demonstrated simply be collected by hand while walking the stream) widespread potential applicability (Leland et al. 2011; and popularity (i.e., to fishers and collectors), long- Kilada et al. 2012). term population impacts are possible, even under light fishing pressure. Based on the above, the species can be Reproduction considered as an unsustainable resource. Euastacus sulcatus is a large species with a Although E. sulcatus is protected in Queensland comparatively moderate fecundity, carrying fewer eggs (Fisheries Queensland 2012), generic fishing regulations (45–600) than the maxima recorded for other large spiny (i.e., those covering all spiny crayfish generally) in NSW crayfishes, such as E. armatus (800), E. bispinosus (812), allow recreational fishers to take five crayfish >90mm OCL E. kershawi (>1000), E. spinifer (1299) and E. valentulus per day (NSW Department of Primary Industries 2012). (>1000), but more eggs than much smaller congeners The regulations thus provide protection for mature such as E. australasiensis (155), E. girurmulayn (50), E. animals between 50 and 90 mm OCL, and in that sense gumar (150), E. hirsutus (84), E. mirangudjin (80) and are sufficient for the species as a whole. Furthermore, E. urospinosus (119) (Clark 1937; Barker 1992; Honan most of the populations should be protected by their & Mitchell 1995c; Morgan 1997; Borsboom 1998; distribution within national park boundaries. However, Honan 1998; Morey 1998; Coughran 2006a, 2011a,b). illegal fishing activities appear to be common (author, Although Morgan (1988) and Furse et al. (2006) noted pers. obs.; Coughran & Furse 2010). It is therefore that the species carried eggs over winter, it appears recommended that NSW fishing regulations are revised that the breeding season in the present study was more to address more specific conditions. For E. sulcatus, the protracted. Mature females emerging in mid-spring pertinent points are that berried females (which this were captured with relatively undeveloped eggs, and study has demonstrated are highly catchable) should given the relatively quick development period observed be returned to the water, and that national parks and for eggs and juveniles (two months) it is likely that the conservation reserves are no-take exclusion zones. breeding cycle was completed in its entirety from spring Increased educational materials (e.g., signage and to early summer. brochures) within national parks, particularly at key It is possible that females over-winter eggs that enter camping and visitation areas, could also help mitigate a diapause stage (i.e., a period during which growth poaching. and development are suspended), as has been noted Although the species appears to be morphologically for the New Zealand species Paranephrops zealandicus similar throughout its range, there were biological (Whitmore & Huryn 1999). However, based on the timing differences recorded for the NSW populations of E. of egg development in the present study, and observed sulcatus in this study compared to previous work on the concurrently on congeners (Coughran 2006a), it seems species: (i) the timing of re-emergence of adults was two more likely that E. sulcatus lays, or at least fertilizes, the months earlier than has been recorded in Queensland; eggs in spring. The inconsistency with the observations (ii) the reproductive period was more protracted, of Morgan (1988) and Furse et al. (2006) might be due to extending from spring to early summer, rather than the effects of environment or location (Turvey & Merrick winter to summer as has been recorded in Queensland; 1997a), or erratic spawning out of season (Clark 1937; (iii) the moulting records suggest a much slower growth Hopkins 1967) in either the Queensland or NSW studies. rate and increased longevity than has been previously It is also possible that the species produces two broods recognised; and (iv) distinct colour variants have been each year, however if this were the case two cohorts of recorded for different highland populations. independent juveniles should have been observed in the In light of these differences, and the restriction of field surveys. the species to distinct highland areas throughout its range, it is recommended that molecular analyses be Implications for Conservation used to assess potential genetic distinctions between The very slow growth rate and apparent longevity populations. If there is any cryptic variation within the of Euastacus sulcatus renders it highly vulnerable to taxon, it is important that this is recognised to facilitate over-fishing, and the mass spawning pattern also leaves conservation. It is also recommended that further these populations susceptible to cohort-wide impacts, research is invested into direct ageing methods for E. particularly given the high catchability of berried sulcatus, and other, slow growing and long-lived spiny females when they re-emerge during late spring. Given crayfish.
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